living (stained) calcareous benthic foraminifera from recent ...interval at the organic-rich and...

403LIVING CALCAREOUS BENTHIC FORAMINIFERA OFF CONCEPCIONRevista Chilena de Historia Natural81: 403-416, 2008

Living (stained) calcareous benthic foraminifera from recent sedimentsoff Concepción, central-southern Chile (~36º S)

Foraminíferos bentónicos calcáreos vivos (teñidos) en sedimentos recientes deConcepción, Chile centro-sur (~36º S)

RAÚL TAPIA1,2, *, CARINA B. LANGE 2,3 & MARGARITA MARCHANT4

1 Programa de Postgrado en Oceanografía, Departamento de Oceanografía, Universidad de Concepción,Casilla 160-C, Concepción, Chile

2 Centro de Investigación Oceanográfica en el Pacífico Sur-Oriental (FONDAP-COPAS), Universidad de Concepción,Casilla 160-C, Concepción, Chile

3 Departamento de Oceanografía, Universidad de Concepción, Casilla 160-C, Concepción, Chile4 Departamento de Zoología, Universidad de Concepción, Casilla 160-C, Concepción, Chile

*e-mail for correspondenc: [email protected]

ABSTRACT

This study examines onshore-offshore and vertical distribution of living (Rose Bengal stained) benthicforaminifera (> 180 μm fraction) from three sediment stations along a bathymetric transect off Concepción,Chile (station 18 = 88 m water depth, station 26 = 120 m, station 40 = 1,030 m), within and below the oxygenminimum zone. All cores were collected in austral winter. Calcareous foraminifera dominated the threestations. The species composition, living foraminifera density, and vertical distribution patterns within thesediment changed in accordance with bottom water dissolved oxygen concentration and food availability.Onshore-offshore pattern revealed overall highest living foraminiferal densities at shelf stations 18 and 26where bottom water dissolved oxygen was lowest (~ 0.2 mL-1) and content in labile organic matter highest.Within the sediment, maximum relative abundances (50-60 %) of living organisms were found in the 0-1 cminterval at the organic-rich and oxygen-poor shelf stations 18 and 26. In the well-oxygenated (2.7 mL-1) slopestation 40, 70 % of living foraminifera were observed deeper than the first centimeter. The number of speciesand the contribution of the > 250 μm fraction to the total fauna larger than 180 μm increased offshore.Nonionella auris (d’Orbigny) dominated at stations 18 and 26 while a more diverse foraminifera fauna wasfound at station 40. This study provides the first quantitative data on living benthic foraminifera in the area;seasonal and interannual changes are not addressed.

Key words: benthic foraminifera, sediments, oxygen minimum zone, Concepción, Chile.

RESUMEN

Este estudio examina la distribución costa-océano y vertical de los foraminíferos bentónicos calcáreos(fracción > 180 μm) vivos (teñidos) en tres estaciones a lo largo de un transecto batimétrico frente al área deConcepción, Chile (estación 18 = 88 m, estación 26 = 120 m, estación 40 = 1.030 m de profundidad), dentro ybajo la zona mínima de oxígeno. Todos los testigos de sedimento fueron recolectados durante el período deinvierno. Los foraminíferos calcáreos dominaron las tres estaciones. La composición específica, distribuciónvertical y abundancia de foraminíferos bentónicos vivos variaron en concordancia con el contenido deoxígeno disuelto del agua de fondo y la disponibilidad de materia orgánica. El patrón batimétrico reveló unamayor densidad de de foraminíferos vivos en las estaciones 18 y 26 donde el oxígeno disuelto de las aguas defondo fue menor (~ 0,2 mL-1) y la materia orgánica lábil mayor. Dentro del sedimento, las máximasabundancias relativas (50-60 %) de foraminíferos vivos fueron encontrados en el intervalo 0-1 cm en lasestaciones 18 y 26 ricas en materia orgánica y pobremente oxigenadas. En la bien oxigenada (2,7 mL-1)estación 40, el 70 % de los foraminíferos vivos se ubicaron por debajo del primer centímetro. El número deespecies y la contribución de la fracción > 250 μm se incrementaron costa afuera. Nonionella auris(d’Orbigny) fue la especie dominante en las estaciones 18 y 26, mientras que una fauna más rica se observóen la estación 40. Este estudio proporciona los primeros datos generales acerca de la distribución deforaminíferos bentónicos vivos en el área, sin apuntar a cambios estacionales y/o interanuales.

Palabras clave: foraminíferos bentónicos, sedimentos, zona de mínimo oxigeno, Concepción, Chile.

404 TAPIA ET AL.

INTRODUCTION

The vertical distribution of benthic foraminifersin the sediment column seems to be determinedmainly by two factors: food availability andoxygen content at the seafloor (Gooday &Rathburn 1999, Gooday 2003). This issupported by a number of field studies andexperiments that demonstrate the effects oforganic supply and changes in bottom wateroxygen concentration on the microhabitatselection (e.g., Rathburn & Corliss 1994, Ernst& van der Zwaan 2004).

All these observations were summarized inthe “TROX-model” of Jorissen et al. (1995),which relates the microhabitat “selection” of agiven taxa to a balance between food andoxygen availability. According to this model,oligotrophic systems are food-limited andorganisms are concentrated close to the sedimentsurface, where the majority of the food islocated. Although eutrophic systems are oxygen-limited, organisms are also concentrated near thesurface in order to avoid anoxic conditionsdeeper in the sediment. This general scheme hasbeen refined by Jorissen (1999), van der Zwaanet al. (1999), and Fontanier et al. (2002) whosuggested that: (1) the organic matter flux is themain parameter controlling foraminiferalmicrohabitats, (2) oxygen is not the limitingfactor for deep infaunal species, and that (3)biological interactions, particularly competitionfor labile food material, may play a role inmicrohabitat selection.

Oxygen minimum zones (OMZs) aresignificant midwater features in the easternPacific Ocean (e.g., Helly & Levin 2004). It hasbeen shown that, where the OMZ intercepts thecontinental margin, strong gradients are formedin both bottom water dissolved oxygenconcentrations and organic matter input (Levin

et al. 2000). These gradients influence thebiogeochemical properties of the underlyingsediments and the distribution of benthicorganisms within the sedimentary column.Usually organic-rich, oxygen-poor environmentsare dominated by meiofauna, mainly calcareousforaminifera and nematodes (e.g., Levin et al.2002). In the last decades, significant advanceshave been made in the understanding ofecological aspects of benthic foraminifera fromoxygen deficient settings in the world (seeBernhard & Sen Gupta 1999 for a review),including off Peru in the eastern south Pacific(Phleger & Soutar 1973, Levin et al. 2002).

Substantial progress in the knowledge ofmodern benthic foraminifera from the Chileancontinental margin has been made since theearly works of Bandy & Rodolfo (1964),Boltovskoy & Theyer (1970), and Ingle et al.(1980). More recent studies (e.g., Zapata &Moyano 1997, Figueroa et al. 2005, 2006,Hromic et al. 2006) have focused on taxonomicand/or biogeographical aspects, emphasizing theidentification and characterization ofzoogeographic provinces along the Chileancoast. But none of these studies investigated therelationship between living benthic foraminiferalfauna and environmental characteristics.

To provide new insight into benthicforaminiferal ecology off Concepción, Chile (~36º S), we present results on total and livingbenthic foraminifera from a bathymetrictransect (80, 120, 1,030 m water depth; Table1, Fig. 1A) that includes stations within(stations 18 and 26) and below the OMZ(statation 40). Our study focused on (1)onshore-offshore, and (2) vertical distributionof calcareous foraminiferal communities withinthe sedimentary column (upper 10 cm) withregard to bottom water oxygen content andorganic matter availability.

TABLE 1

Location and collection date of sampling sites

Localización de las estaciones y fechas de muestreo

Station Core Collection date Latitude (S) Longitude (W) Water depth (m)

18 MUC1803 12 August 2003 36º30’ 73º07’ 88

26 MUC2603 12 August 2003 36º26’ 73º23’ 120

40 RC4004 10 August 2004 36º20’ 73º44’ 1.030

MUC = Multicorer, RC = Rhumor corer

405LIVING CALCAREOUS BENTHIC FORAMINIFERA OFF CONCEPCION

Regional setting

The area off central-southern Chile has beenstudied in detail by various authors (Ahumada& Chuecas 1979, Sobarzo et al . 2001)including plankton variability, biogeochemicalprocesses, and physical and chemicalcharacteristics (Escribano & Schneider 2007).

Due to diverse factors (coastal winds,upwelling events, shelf width, and topographicsettings), this area is one of the most productivesectors of the central-southern Chilean coast(35-45º S, Shaffer et al. 1999) with primaryproductivity values among the highest in theworld ocean (Daneri et al. 2000, Schubert et al.2000). Upwelling is strongly seasonal. It

intensifies during austral spring-summer,fertilizing the photic zone with the salty,nutrient-rich, oxygen-poor waters of theEquatorial Subsurface Water mass (ESSW)(Ahumada & Chuecas 1979). Upwelled ESSWcan be found over the continental shelf andsometimes even at the inner part of ConcepciónBay. Downwelling usually occurs in winter dueto the prevalence of strong northerly winds(Sobarzo 1993).

High phytoplankton biomass and primaryproduction (reaching 19.9 g C m-2 d-1, Daneri etal. 2000) followed by high rates of organicmatter sedimentation to the seafloor (e.g.,Gutiérrez et al. 2000) promote anoxic/dysoxicconditions in the sediments (Neira et al. 2001).

Fig.1: (A) Study area showing the position of the sampling stations off Concepción used in thisstudy: station 18 (middle shelf), 26 (outer shelf), and 40 (on the middle slope), and bathymetry; (B)T-S diagram (April 2003) for station 40 showing the different water masses present: SubantarcticWater (SAAW), Equatorial Subsurface Water (ESSW), and Antarctic Intermediate Water (AAIW).See text for details.(A) Área de estudio mostrando la posición de las estaciones de muestreo frente a Concepción utilizadas en este estudio:estaciones 18 (plataforma interior), 26 (plataforma exterior), y 40 (talud), y batimetría de la región; (B) diagrama T-S (abril2003) para la estación 40 mostrando las diferentes masas de agua presentes: Agua Antárctica Superficial (SAAW), AguaEcuatorial Subsuperficial (ESSW) y Agua Intermedia Antárctica (AAIW). Ver texto para detalles.

406 TAPIA ET AL.

Total organic carbon content (TOC) in thesediment is usually high and varies between 2and 5 % (Table 2), with maximum TOC valuesin austral summer (Muñoz et al. 2007). Organicmatter is mainly of phytoplanktonic origin(Schubert et al. 2000). Chlorophyll-a (Chl-a)concentrations in the surface sediments clearlydecrease offshore (Table 2). On a yearly basis,C/N molar values fluctuate between 8.4 and11.3 (Muñoz et al . 2007). Modernsedimentation rates are high (0.09-0.25 cm yr-1,Muñoz et al. 2004). Sediments are usuallycomposed of silt and clay minerals with a meangrain size of 8.5-13.0 μm (Molina et al. 2004).

The study area is located on the widestportion of the continental margin off central-southern Chile (50 km) (Fig. 1A). The shelf islimited by two submarine canyons and theircorresponding rivers: the Itata canyon (ItataRiver) to the north and the Biobío canyon (Bio-Bío River) to the south. In general, threedifferent water masses can be observed here:Subantarctic Water (SAAW) between thesurface and about 80 m depth, ESSW at about80 to 400 m with minimum dissolved oxygenconcentrations, and Antarctic IntermediateWater (AAIW) below 400 m (Molina et al.2004) impinging on the continental slope (Fig.1B). The OMZ is associated with oxygen-depleted ESSW and intensifies by the localbiogeochemical O2 consumption (Paulmier etal. 2006). Off Concepción, the OMZ is lessintense and its upper boundaries are deeper(about 100 m) than off northern Chile (Pizarroet al. 2002); its strength and the depth of theupper boundary vary seasonally. The OMZ’supper boundary is shallow in spring-summer (at20 m from October to March) during the highupwelling activity period with O2concentrations lower than 0.2 mL-1, but itdeepens in autumn (about 50 m in April-May)(Paulmier et al. 2006).

MATERIAL AND METHODS

The sediment samples used in this study werecollected during winter cruises as part of theCOPAS Center Time Series Study offConcepción (Table 1). A SMBA-type mini-multicorer (MUC) with six sampling tubes(inner diameter = 9.5 cm) was used forsampling at Sta. 18 (middle shelf, 88 m water

depth) and 26 (outer shelf, 120 m water depth)(Fig. 1A). A Rhumor corer (RC) - a type ofgravity corer that recovers the sediment-waterinterface - was used at Sta. 40 (middle slope,1,030 m water depth). The RC uses an acrylicof 7 cm internal diameter and ~ 100 cm inlength. One core tube was analyzed for eachstation. Due to the limited data set, interannualand seasonal changes cannot be addressed.

The cores were sliced at 0.5 cm intervals forthe upper 2-3 cm, and every 1 cm downcore.Immediately after slicing, the samples werepreserved and stained according to themethodology of Rathburn & Corliss (1994);samples were allowed to stain for at least oneweek before processing for foraminiferaanalysis. Samples were not split but examinedentirely for their content of live foraminifera.The use of Rose Bengal stained foraminifera tointerpret living associations was criticallydiscussed by Bernhard (1988). One problem ofthis technique is the fact that Rose Bengal maystain the protoplasm of dead foraminifera, whichmay be relatively well preserved under anoxicconditions leading to an overestimation of theliving fauna. However, it is still the mostfrequently used method in foraminifera researchand the most practical one (Bernhard 2000). Ourdefinition of “stained” (living) foraminifera wasvery strict and only specimens with allchambers, except for the last one (the youngest)stained bright pink were counted as stained.

After staining, samples were wet-sievedusing 63, 180, and 250 μm mesh-opening. Thedata presented here are from the > 250 and 180-250 μm fractions and refer to the upper 10 cmof each core. The mesh sizes were selected inkeeping with the methodology previously usedfor the COPAS Time Series Study offConcepción (Tapia 2003). The fraction 63-180μm was preserved for future studies.

We are aware of the fact that the selectionof the > 180 μm size fraction may haveintroduced some bias regarding the abundanceof total foraminifers as well as the abundanceof smaller organisms. Although the smaller sizefraction (e.g., 63-150 μm) may contain a largenumber of foraminiferal species and juvenileforms that are rare or absent in the larger sizefraction (e.g., Schröder et al. 1987), theirremoval is extremely time-consuming.Additionally, smaller specimens are often moreproblematic to identify to the species level.


To our knowledge, there is only onequantitative (unpublished) study of livingbenthic foraminifera available for the shelf offConcepción (Mayor et al. unpublished results).Our results may have underestimated the totalnumber of living foraminifera in the study area(shelf stations) by ca. 20 % as compared withthe abundances obtained by Mayor et al.(unpublished results) for the > 150 μm fraction.However, the total numbers of benthicforaminifera (stained + dead) and species thatwe found for the slope area off Concepciónfalls within the range obtained by Figueroa etal. (2005, 2006) who analyzed the > 150 μm atnearby slope and deep stations. An importantaspect is that a scan of the > 63 μm fractionrevealed that, with the exception of tinyGlobobulimina and Stanforthia, the overallspecies composition for the Concepción area iscomparable in both small and coarser sizefractions.

The total density of living calcareousforaminifera was determined by integrating thenumbers of live individuals picked at all levelsfrom 0 to 10 cm sediment depth. Percentages ofindividual taxa were calculated from the rawdensity data. Concerning vertical profiles,

foraminiferal densities were normalized to 50cm3 sediment volume for each 0.5 and 1 cmlayer. Finally, with the purpose of comparisonwith other areas, living calcareous foraminiferawere normalized to 50 cm2 for the firstcentimeter.

We assigned the benthic foraminifera to twodifferent microhabitat groups (shallow anddeep infauna). None of the species offConcepción could be considered to be strictlyepifauna as defined by Buzas et al. (1993) whosuggested that only species living on elevatedsubstrates can be assigned to this category.

In order to provide an overview of theenvironmental characteristics in the study area,we present available water column and surfacesediment data in Table 2; in those cases whenenvironmental data were not available for thedates we collected the cores, we resorted topreviously published data. Water column dataderive mostly from the COPAS Time SeriesStudy off Concepción (http://copas.udec.cl/eng/research/timeseries.php), and include CTDOdata (2002-2004) and/or data obtained fromNiskin bottles (station 40). The sediment datastem from several sources (Gutiérrez 2000,Gallardo et al. 2004, Muñoz et al. 2007).

TABLE 2

Summary of available water column and surface sediment characteristics off Concepción

Resumen de la características de la columna de agua y sedimentos para el área frente a Concepción

Water column Station

18(88 m) 26(120 m) 40(1,030 m)

Summer Winter Summer Winter Summer Winter

Bottom water dissolved oxygen (mlL-1) 0.071 0.451 (0.17)a 0.42 0.62 3.41 2.91 (2.7)b

Surface water temperature (ºC) 13.31 12.51 (11.8)a nd 14.61 12.31

Bottom water temperature (ºC) 10.51 10.81 (11.2)a 9.22 11.62 4.61 4.01

Surface water salinity (psu) 32.21 32.91 (32.8)a nd 33.81 34.71

Bottom water salinity (psu) 34.61 34.51 (34.6)a 35.92 35.12 34.21 34.31

Sediments Middle shelf Outer shelf Middle slope

Chlorophyll-a (μg g-1) * 24.13 21.93 (8.1)3 28.72 27.92 13.44 nd

% TOC * 3.93 3.32 4.62 5.12 2.95 2.14

Eh (mV) * 1202 1682 1762 1392 2574 nd

Sources: 1CTDO data (2002-2004) (http://copas.udec.cl/eng/research/timeseries.php) from COPAS Time-Series offConcepción averaged for summer and winter seasons; 2Gutiérrez (2000), includes data within the El Niño 1997-98 period;3Muñoz et al. (2007); 4Gallardo et al. (2004); 5Böning et al. (2005). Data in parentheses refer to the sampling time of thisstudy, based on CTDO profiles (a) or Niskin bottles (b); (*) data for the first centimeter of sediment; nd = no data available.Bottom water oxygen and temperature measured at 80 m depth at station 18, and at 750 m depth at Station 40

408 TAPIA ET AL.

RESULTS

The sediments off Concepción weretypically greenish-brown in color (7.5 Y 3/2-7.5 Y 4/2 Munsell table color). Fecal pelletswere numerous at the shallower stations (Sta.18 and 26). A grey layer of very fine materialwas observed at 7-9 cm depth in the core fromstation 40. Available Chl-α and TOC data(although not always coincident with ourAugust samplings) reveal that the sediments ofthe shelf stations are generally characterizedby higher levels of Chl-a concentrations andTOC (> 20 μg g-1 and > 3.3 %, respectively)than the slope station 40 (Table 2). Bottomwater dissolved oxygen (BWDO) conditionsdiffered along the transect. Minimum BWDOvalues (0.17 mL-1) were encountered at station18 (88 m water depth) and maximum values atstation 40 (2.7 mL-1) during our Augustsamplings (Table 2), in agreement with knownOMZ boundaries in the area. Redox potentialvalues at the sediment surface (Eh) agree withincreasing bottom water dissolved oxygenconcentrations from onshore to offshore(Table 2).

Using the BWDO values given in Table 2,the stations could be grouped into two

categories according to Sen Gupta & Machain-Castillo (1993) classification of environments:(1) shelf stations 18 and 26, with dysoxic-suboxic conditions (< 2 mL-1), located at andimmediately below the upper boundary of theOMZ, respectively; and (2) slope station 40,with oxygenated conditions (> 2 mL-l), locatedseveral hundred meters below the OMZ.Bottom water temperature, salinity, and BWDO(Table 2) showed the influence of the ESSW atSta. 18 and 26, whereas AAIW affected Sta. 40.

Onshore-offshore distribution of benthicforaminifera

The analysis of benthic foraminifera in thecores off Concepción showed that thecontribution of the > 250 μm fraction to thetotal fauna (larger than 180 μm) increasedoffshore (Table 3) from 1.8 % (88 m) to 16 %(120 m) and 29 % (1030 m water depth).

At all three stations, rotalid foraminiferawere the main component of the total benthicforaminiferal fauna (> 75 %). Agglutinatedforaminifera were very rare (0.4 %) at Sta. 18but reached 8 and 16 % of the total fauna atstation 26 and 40, respectively. Miliolids wereonly present at station 40 (~ 1 %) (Table 3).

TABLE 3

Size range of benthic foraminifera, relative abundance of the three main groups (Agglutinated,Rotalid and Miliolid in the > 180 μm fraction), total number of living species, percentage of livingcalcareous foraminifera with respect to total benthic foraminifera, and total benthic foraminifera

(> 180 μm, calcareous + agglutinated) within the upper 10 cm of each core at stations 18, 26and 40. Totals are standardized to 50 cm2 surface area and 10 cm sediment depth

Rango de tamaño de los foraminíferos bentónicos, abundancia relativa de los tres principales grupos (Aglutinados,Rotalidos y Miliolidos en la fracción > 180 μm), número de especies vivas, porcentaje de foraminíferos bentónicos

calcáreos vivos con respecto al total de bentónicos, y foraminíferos bentónicos totales (> 180 μm, calcáreos + aglutinados)dentro de los primeros 10 cm de cada testigo de sedimento para las estaciones 18, 26 y 40. Los totales están estandarizados

a 50 cm2 de superficie y 10 cm de profundidad de sedimento

Characteristic Station 18(88 m) Station 26(120 m) Station 40(1,030 m)

Size range > 250’μm (%) 1.8 16 29

250-180 μm (%) 98.2 84 62

Main groups Rotalid foraminifera (%) 99.6 92 83

Agglutinated foraminifera (%) 0.4 8 16

Miliolid foraminifera (%) 0 0 ~ 1

Total number of living species 3 10 18

Percentage of living Living calcareous foraminifera (%) 60 18 7

Total benthic foraminifera 615 1,904 5,252


Table 4 provides the listing of all livingbenthic foraminifera species found in thisstudy. Stations 18 and 26 shared the same livecalcareous assemblage. Both stations werecharacterized by the dominance of Nonionellaauris (d’Orbigny), which made up > 90 % ofthe total fauna of stained calcareousforaminifera (Table 5). In contrast,foraminiferal live assemblage at station 40strongly differed. Here, Bolivina spissaCushman, Globobulimina affinis (d’Orbigny),Chilostomella oolina Schwager, and Uvigerinaperegrina Cushman were the most relevant taxa(Table 5).

The relative abundance of stainedcalcareous foraminifera (> 180 μm, Table 3) aswell as their densities within the firstcentimeter (Table 6) decreased drastically fromshelf to slope (i.e., from 161-198 at shelfstations 18 and 26 to 96 specimens per 50 cm2

at Sta. 40).

Downcore pattern and microhabitat of benthicforaminifer species

Stations 18 and 26 showed the highestconcentrations of stained organisms near the

sediment surface (Fig. 2); indeed, 50 and 60 %(cumulative percent) of total living calcareousforaminifera were observed within the firstcentimeter at each station. In contrast, station40 contained only 30 % of the total stainedcalcareous foraminifera at the surface, and amaximum was observed at 1-1.5 cm (~ 22 % oftotal living calcareous foraminifera) (Fig. 2). Inaddition, minor secondary abundance peakswere observed at station 18 and 40 between 5-6cm (~ 5 %) and 3-4 cm (~ 9 %), respectively(Fig. 2).

Identification of species microhabitat wasbased on the presence or absence of an infaunalmaximum, and on the shape of the distributionprofile of each species (position with respect toother taxa; Fig. 3). Based on these assumptions,we defined the species N. auris, B. spissa, U.peregrine, B. seminuda and B. costata asshallow infauna, and G. affinis and C. oolina asdeep infauna. The high abundance of shallowinfauna and the absence of deep infaunacharacterized the shelf stations located underthe OMZ’s influence (station 18 and 26). Incontrast, shallow and deep infaunal specieswere observed at the slope station 40 (1,030 mwater depth).

TABLE 4

Living (stained) benthic foraminifers identified in this study

Foraminíferos bentónicos vivos (teñidos) identificados en este estudio

Bolivina costata d’Orbigny, 1839.

Bolivina plicata d’Orbigny, 1839.

Bolivina seminuda Cushman = Bolivina seminuda var. humilis Cushman and McCulloch, 1942.

Bolivina spissa Cushman = Bolivina subadvena Chusman var. spissa Chusman, 1926.

Bulimina denudata Cushman and Parker, 1938.

Cassidulina limbata Cushman and Hughes 1925.

Chilostomella oolina Schwager 1878.

Cibicidoides wuellerstorfi (Schwager, 1866) = Cibicidoides wuellerstorfi Resig ,1981.

Dentalina communis (d’Orbigny) = Nodosaria (Dentilina) communis d’Orbigny, 1826.

Epistominella pacifica (Cushman) = Pulvinulinella pacifica Cushman, 1927.

Gyrodinoides neosoldanii (Brotzen) = Gyroidina neosoldani Ingle et al., 1980.

Globobulimina affinis (d’Orbigny) = Bulimina affinis d’Orbigny, 1839.

Martinottiella communis (d’Orbigny) = Clavulina communis d’Orbigny, 1826.

Melonis barleeanum (Williamson) = Nonionina barleeana Williamson, 1858.

Nonionella auris (d’Orbigny) = Valvulina auris d’Orbigny, 1839.

Pyrgo murrhina (Schwager, 1866) = Pyrgo murrhyna Resig, 1981.

Sacammina atlantica (Cushman) = Proteonina atlantica Cushman, 1944.

Uvigerina peregrina Cushman, 1923.

410 TAPIA ET AL.

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00

00

10

00

00

51

Sta

tion

26

N.

auri

s14

011

511

539

178

73

13

10

449

SI

92.8

B.

sem

inud

a2

102

10

00

00

00

015

SI

3.1

B.

c ost

ata

42

11

00

00

00

00

8S

I1.

6

Oth

e rs

42

32

10

00

00

00

122.

5

Sta

tion

40

0-0.

5 cm

0.5-

1 cm

1-1.

5 cm

1.5-

2 cm

2-2.

5 cm

2.5-

3 cm

3-4

cm4-

5 cm

5-6

cm6-

7 cm

7-8

cm8-

9 cm

9-10

cm

Tot

a l n

umbe

rM

hP

e rc e

nta g

e of

tot

a lli

ving

for

ams

c alc

a re o

us l

ivin

g fa

una

B.

spis

sa31

2649

184

317

18

40

01

162

SI

57.5

G.

affi

nis

23

42

79

147

28

10

261

DI

21.6

C.

ooli

na4

40

14

28

44

20

00

33D

I11

.7

U.

pere

grin

a1

21

31

00

00

00

00

8S

I2.

8

Oth

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10

15

21

80

00

00

018

6.4


TABLE 6

Number of species and density data for living (stained) benthic foraminifera from low-oxygenenvironments (modified from Gooday 2003), compared to our study area. ND = no data

Número de especies y densidad de foraminíferos bentónicos vivos (teñidos) de ambientes pobres en oxígeno (modificadode Gooday 2003) comparados con nuestra área de estudio. ND = sin datos

Site and depth BWDO (mL-1) Number Stained specimens Reference; size fraction andof species per 50 cm2 horizon examined

Oman margin Gooday et al. (2000)> 63 μm, 0-1 cm

412 m 0.13 64 65,535

3,350 m ~ 3.00 208 2,930

Santa Barbara basin Phleger & Soutar (1973)> 62 μm, surface sediment

575 m ~ 0.1 ~ 13 5,875

590 m ~ 0.1 ND 5,250

Santa Barbara basin Bernhard (1990)> 63 μm, 0-1 cm

486 m (Feb 1988) ~ 0.11 ND 2,660

550 m (June 1888) < 0.1 ND 34,505

550 m (Feb 1988) < 0.1 ND 21,700

550 m (June 1988) < 0.1 ND 47,785

550 m (Oct 1988) 0.01 ND 48,130

550 m (July 1989) Anoxic ND 135

Santa Barbara basin Bernhard et al. (1997)> 63 μm, 0-1 cm

339 m 0.51 7 2,660

431 m 0.35 11 34,505

522 m 0.08 10 9,430

537 m 0.04 12 6,350

591 m 0.06 9 19,790

Point Conception Shepperd et al. (2007)> 150 μm, 0-1 cm

990 m (May 1996) 0.47 3 188

990 m (Aug 1996) 0.46 3 308

990 m (Oct 1996) 0.44 7 246

Callao (Perú) Phleger & Soutar (1973)> 62 μm, surface sediment

180 m ND ~ 11 ~ 3,000

Callao (Perú) Levin et al. (2002)> 150 μm, 0-1 cm

305 m 0.02 ND 29,043

563 m 0.26 ND 926

831 m 0.84 ND 497

1,211 m 1.78 ND 96

Concepción (Chile) This study> 180 μm, 0-1 cm

88 m (August 2003) ~ 0.2 3 161

120 m (August 2003) ND 10 198

1030 m (August 2004) > 2 18 96

412 TAPIA ET AL.

DISCUSSION AND CONCLUSIONS

We are aware that the conclusions we can drawfrom our study are limited by the reducedsampling occasions and by the size fractionselected (> 180 μm), which may haveintroduced some bias regarding to theabundance of total foraminifers. Nevertheless,these data provide valuable insights into theecology of foraminifera in the region and thetrends indicated by our foraminiferal data mayserve as groundwork for future testing.

Despite the methodological differences, our0-1 cm density data of stained specimens(standardized to 50 cm2) are comparable to thevalues observed off Point Conception,California, by Shepperd et al. (2007) andsuboxic slope settings off Callao, Peru, byLevin et al. (2002), who used size fractions >150 μm (Table 6). Our data are lower thanthose reported for the oxygen-poor SantaBarbara Basin (Bernhard 1990, 1992) and muchlower than the Arabian Sea, where densities oftens of thousands of living benthic foraminifera(fractions > 63 and 150 μm) have been found in

Fig.2: Vertical distribution of total living benthic calcareous foraminifers (Rose Bengal stained,fraction > 180 μm, standardized to 50 cm3 sediment volume), and cumulative percent of livingorganisms within the upper 10 cm of each core.Distribución vertical de los foraminíferos calcáreos vivos totales (teñidos con Rosa de Bengala, fracción > 180 μm,estandarizados a 50 cm3 de sedimento) y porcentaje acumulado de organismos vivos dentro de los primeros 10 cm de cadatestigo de sedimento.

surface sediments influenced by low oxygenconditions (Gooday et al. 2000) (Table 6).

According to Sen Gupta & Machain-Castil lo (1993), about ten calcareousforaminifer species typically live in oxygen-poor areas, with two or three species usuallycomprising as much as 80 % of the fauna. Inour study, the number of living calcareousspecies for shelf stations 18 and 26 variedbetween 3 and 10 (Table 3 and 6); ~ 90 % ofthe total calcareous living benthic foraminiferalfauna were composed by one species (Table 5).The number of species is similar to that foundin the Santa Barbara basin, California, byPhleger & Soutar (1973) and Bernhard et al.(1997), who reported 7-13 stained species ofcalcareous foraminifera in the > 63 μm fraction(Table 6), and to Peru, where one species(Bolivina cf. pacifica) composes > 95 % of theliving fauna (Phleger & Soutar 1973). Incontrast, our data are much lower than thosereported for the Oman Margin, where the totalnumber of stained species observed by Goodayet al. (2000) varied between 49 (> 125 μm) and64 (> 63 μm).

(Number 50 cm-3)


Fig.3: Vertical distribution of the most important taxa of living benthic calcareous foraminifers(Rose Bengal stained, fraction > 180 μm, standardized to 50 cm3 sediment volume) within theupper 10 cm of each core.Distribución vertical de las especies de foraminíferos calcáreos vivos más importantes (teñidos con Rosa de Bengala,fracción > 180 μm, estandarizados a 50 cm3 de sedimento) dentro de los primeros 10 cm de cada testigo de sedimento.

Onshore-offshore distribution of l ivingforaminifera

It is well known that benthic foraminiferalabundances in marine sediments are closelyrelated to food availability, and foraminiferagenerally prosper where food is abundant(Gooday et al. 2000). Along our transect, wedetected a decreasing trend in living foraminifera(> 180 mm) within the first centimeter withincreasing water depth (from 161-198 at stations18 and 26 to 96 specimens per 50 cm2 at station40, Table 6). This is most probably induced bylower and less labile organic matter flux reachingthe sea floor in deeper settings such as those ofSta. 40 (Schubert et al. 2000, Molina et al. 2004,Muñoz et al. 2004), and/or a reduction inpredation pressure at oxygen-depleted settingssuch as stations 18 and 26 (Gooday 2003).Although available Chl-α and TOCmeasurements do not coincide with the samplingtimes for foraminifera, on hand data show thatstation 40 is generally characterized by lowerlevels of Chl-α concentrations and TOC (~ 13mg g-1 and < 3 %, respectively) than the shelfstations (Table 2).

In order to gain access to food, benthicforaminifers must tolerate the oxygen depletionthat frequently accompanies abundant organicmatter. Reduced oxygen concentrations and/orrecurring anoxia events will influence the sizedistribution and taxonomic composition offoraminiferal assemblages, eliminating the lesstolerant species, whereas abundance anddominance increase for the remaining species(Sen Gupta & Machain-Castillo 1993, Goodayet al. 2000). Our observations are consistentwith these concepts, showing minimal presenceof large foraminifera and the dominance of alow diversity assemblage in the oxygen-poorconditions of the shallowest stations (18 and26), which are associated with the upperboundary of the OMZ. Here, the shelfrestricted N. auris (Resig 1981) (in fraction >180 μm, Table 5) composed over 90 % of thetotal living calcareous foraminifera fauna. Aquick scan of the > 63 μm fraction revealedthat N. auris was dominant (data not shown) atthese shelf stations and was accompanied byjuvenile bolivinids (about 30 %) at station 26.

The dominance of N. auris at the twostations associated with the OMZ differs from

414 TAPIA ET AL.

observations by Ingle et al. (1980), who foundtypical OMZ foraminiferal fauna (> 250 μmfraction) in central Chile to be primarilycomposed by bolivinids such as Bolivinaseminuda and Bolivina costata. Bolivinids hada minimal presence or were absent in the 180μm fraction at Sta. 18 and 26 and, as statedabove, juveniles were only observed in the > 63μm fraction at station 26. The discrepancybetween our data and those of Ingle et al.(1980) may be explained by the fact thatbolivinids are commonly associated with stableOMZ conditions (Heinze & Wefer 1992),which is not the case for our study area with aseasonally variable OMZ (Paulmier et al.2006). In contrast, the living assemblageobserved at station 40 (dominated by B. spissa,G. affinis, U. peregrina, C. oolina) agrees withthe one reported previously by Ingle et al.(1980) at similar water depths.

Vertical distribution of living foraminiferalfauna within the upper sediment column (10 cm)

The relationship of the benthic foraminiferalmicrohabitat with food availabili ty andoxygenation of the benthic realm has beenschematized in a conceptual model by Jorissenet al. (1995). The TROX-model explains that,in oligotrophic environments, species adaptedto low organic flux conditions will thrive closeto the sediment-water interface in a well-oxygenated setting. The low flux of organicmatter to the sediment prevents colonization ofthe deeper sediment layers by infaunal taxa. Ineutrophic conditions, on the other hand, wherethe principal redox front is positioned close tothe sediment surface, infaunal taxa are limitedto the first millimeters or centimeters of thesediment (Murray 2001); in this case, they haveonly a limited tolerance for low oxygenconditions.

Faunal penetration is maximal in“mesotrophic” settings because the oxygenpenetration is relatively deep and more or lesslabile food particles are introduced at depth inthe sediment by bioturbating macrofaunacreating suitable microhabitats for benthicforaminifera (Jorissen 1999, Fontanier et al.2002). In such environments, the subsurfaceaccumulation of organic matter (Rathburn &Corliss 1994) and/or grazing on populations ofanaerobic bacteria associated with redox

boundaries (Fontanier et al. 2002) couldexplain the microhabitat selection of a givenforaminifer.

In general terms, the vertical patternsobserved at our stations agree with the TROX-model. At stations 18 and 26, the livingforaminifera are located preferentially near thesediment surface (50 and 60 % of the total livingforaminifera within the first centimeter, Fig. 2).Particularly, species tolerant to low oxygenconditions with shallow infaunal microhabitatpreferences (Bernhard & Sen Gupta 1999) atstations 18 and 26 indicate eutrophic conditions.On the other hand, the deepest penetration offoraminiferal fauna at station 40 is more typicalof mesotrophic conditions (70 % of total livingcalcareous foraminifera occur below the firstcentimeter). Here, an important proportion of theliving population is composed of deep infaunalspecies such as G. affinis (~ 22 %) and C. oolina(~ 12 %) (Table 5). This general scenario wouldsuggest that BWDO is the main controllingagent at stations 18 and 26, whereas food supplycontrols the distribution of benthic foraminiferaat station 40.

The extensive vertical distribution of N.auris at station 18, even with a small peak ofstained organisms in the 5-6 cm level (Fig. 2),is interesting to note. This feature may havetwo explanations. On the one hand, it couldrefer to an artifact of the Rose Bengal methodwhich may have stained the protoplasm of deadforaminifera (Material and Methods section) atthis shallow station. On the other hand, it maybe explained by the strong seasonal variation inbioturbation affecting the upper 2-5 cm of thesediment column associated with highlyseasonally variable BWDO concentrations andorganic matter supply (Muñoz et al. 2007,Table 2). In fact, 210Pb activity profiles show anaverage mixed layer depth of 5 cm at station 18(Muñoz et al. 2007). An additional factor to thepattern observed at station 18 could include thedenitrification capabilities of N. cf stella (mostprobably N auris, according to publishedphotographs, Risgaard-Petersen et al. 2006)which, although pushed deeper down thesedimentary column by bioturbation, wouldallow them to remain alive.

In summary, our results show that a cleardifference exists between shelf stations 18 and26 which are dominated mostly by one speciestolerant to oxygen depletion, and slope station


40 where oxygen availabili ty and foodintroduction within the sediment allow theoccurrence of shallow and deep infaunalspecies.

ACKNOWLEDGEMENTS

We thank the crew of the L/C Kay Kay and theCOPAS technicians for the collection ofsediment samples, and S. Nuñez (UdeC) forcomments during the preparation of thismanuscript. Comments and suggestions by Dr.A.E. Rathburn, and two anonymous refereesgreatly improved the final version of thismanuscript. We acknowledge MECESUPUCO0002 for a scholarship to R. Tapia. Thiswork was funded by the FONDAP-COPASCenter (Project No. 150100007).

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Associate Editor: Patricio CamusReceived September 9, 2007; accepted May 7, 2008

living (stained) calcareous benthic foraminifera from recent ...interval at the organic-rich and...

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